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Vitis Vinifera) Jason P Londo et al. Horticulture Research (2018) 5:10 DOI 10.1038/s41438-018-0020-7 Horticulture Research ARTICLE Open Access Divergence in the transcriptional landscape between low temperature and freeze shock in cultivated grapevine (Vitis vinifera) Jason P. Londo1,2, Alisson P. Kovaleski2 and Jacquelyn A. Lillis1,3 Abstract Low-temperature stresses limit the sustainability and productivity of grapevines when early spring frosts damage young grapevine leaves. Spring conditions often expose grapevines to low, but not damaging, chilling temperatures and these temperatures have been shown to increase freeze resistance in other model systems. In this study, we examined whole-transcriptome gene expression patterns of young leaf tissue from cuttings of five different grapevine cultivars, exposed to chill and freeze shock, in order to understand the underlying transcriptional landscape associated with cold stress response. No visible damage was observed when grapevine leaves were exposed to chilling temperatures while freeze temperatures resulted in variable damage in all cultivars. Significant differences in gene expression were observed between warm control conditions and all types of cold stress. Exposure to chill stress (4 °C) versus freezing stress (−3 °C) resulted in very different patterns of gene expression and enriched pathway responses. Genes from the ethylene signaling, ABA signaling, the AP2/ERF, WRKY, and NAC transcription factor families, and starch/sucrose/galactose pathways were among the most commonly observed to be differentially regulated. Preconditioning leaves to chill temperatures prior to freezing temperatures resulted in slight buffering of gene expression responses, suggesting that differences between chill and freeze shock perception complicates 1234567890():,; 1234567890():,; identification of candidate genes for cold resistance in grapevine. Overall, the transcriptional landscape contrasts observed between low temperature and freezing stresses demonstrate very different activation of candidate pathways impacting grapevine cold response. Introduction restricting production to cultivars that can survive winter Environmental stresses are the leading factors limiting or through production of hybrid varieties. In addition, the current and future expansion of grapevine production increased variation in fall and spring weather patterns can in the United States. As a Mediterranean-adapted species, lead to frost and freeze damage as vines are preparing for cultivated grapevine (Vitis vinifera) is best suited to cli- winter in autumn, and also in spring, as buds exit dor- mates with mild winter conditions and with relatively mancy and tender new growth is present. Frost risk is a consistent temperature change in autumn and spring. constant concern for fruit crop production as young green However, grapevine is often grown outside of this climatic leaves lack the physical defenses associated with freeze niche in regions that have severe winter conditions, resistance during dormancy (freeze barriers and dehy- – drated tissues)1 3. There is no indication that winter variability will cease, thus there is a great need for better Correspondence: Jason P. Londo ([email protected]) 1United States Department of Agriculture, Agricultural Research Service, Grape understanding of grapevine chill and freeze exposure Genetics Research Unit, 630 W. North Street, Geneva, NY, USA response in order to identify candidate genes for future 2 School of Integrative Plant Science, Horticulture section, Cornell University- breeding of hybrid varieties suited for these challenging New York State Agricultural Experiment Station, 630 W. North Street, Geneva, NY, USA growing conditions. Full list of author information is available at the end of the article © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Londo et al. Horticulture Research (2018) 5:10 Page 2 of 14 Studies of freeze shock (<0 °C) and chill shock (4–10 °C) As a result of these studies, different grapevine cultivars stresses in a number of different crop and plant species and grapevine species have been ranked as cold hardy have resulted in a common cold response (COR) gene or cold tender. The majority of transcriptomic studies regulation and signaling cascade. While a temperature examining cold-temperature effects in grapevine involve – sensor has yet to be confirmed, plants are able to perceive studies of leaf or berry tissue19 23. During these studies, low temperature and initiate a gene regulation cascade cold stress is often applied as low, non-freezing that prepares the plant to tolerate or resist freeze damage. temperatures such as 4 °C. These studies have demon- This cascade begins with the activation of calcium sig- strated a interconnected web of gene regulation shared naling, triggering downstream MAPK kinase activity4, 5, with aspects of drought and salt stresses as well as hor- and changes in the activity of the BHLH transcription mone responses and biotic stress10. Cold stress results in factor family ICE. These ICE genes, in turn, bind to DNA the activation of hundreds of genes with the vast majority and activate the expression of the cold-binding factor/ of their function related to changes in transcription fac- dehydration responsive element-binding (CBF/DREB) tors and activation of genes with poorly annotated – transcription factors6 8. CBF/DREB genes in turn bind to information. These studies are important for under- the DNA and activate many other downstream genes, standing the transcriptional response and potential miti- called COR genes, leading to changes in cryoprotectant gation pathways associated with cold stress damage, but levels and sugar metabolism, as well as impacts on growth they have not been conducted under freezing conditions. and cell expansion9, 10. The elements of this CBF response Further complicating the issue, comparisons of cold have been observed across the plant kingdom and several “hardy” and “sensitive” genotypes may not reflect actual – of the key genes have been identified in grapevine11 13. leaf freezing response as these phenotypic designations Many plants go through a process called acclimation are due to the resistance of dormant tissues, not green when they are exposed to low, but non-freezing tem- growing tissues. peratures. This process is believed to contribute to Studies have been conducted to examine specific gene enhanced freezing resistance by giving the plant time to families (e.g., WRKY) involved in cold stress response24 or adjust its physiology to resist the stresses of ice formation, on whole-transcriptome analysis of low-temperature such as changes in membrane structure, alterations in stress in grapevine comparing cultivated and wild spe- sugar concentrations, and production of cryoproteins14. cies21, but no analysis of the transcriptomic landscape has Studies in Arabidopsis have demonstrated an enhance- been conducted to elucidate the potential differences ment of freeze tolerance and survival after exposing plants between low temperature and freeze stresses in grapevine. to an acclimating temperature of 4 °C for 24 h. However, a Therefore, the objective of this study was to identify previous study in grapevine demonstrated that pretreat- transcripts and pathways that are differentially expressed ment of swollen buds with the same acclimating tem- in young leaf tissue, and enriched in response to various perature was not effective at reducing freeze damage15. cold stresses. We test the hypothesis that exposure to low Few other studies have been conducted to examine the temperature increases freeze resistance in grapevine using potential resistance of grapevine growing tissues to cold contrasts between temperature exposures to explore the temperatures or to examine variation in freeze response of primary transcriptomic processes associated with accli- leaves. The leaves of grapevine are not considered parti- mation/chill (4 °C) exposure, freeze shock (−3 °C), and cularly freeze resistant, typically suffering damage at freeze shock after acclimation (4 to −3 °C). Pathway temperatures below −2.5 °C15. Studies examining frost enrichment analysis was applied to this data to identify protectants have demonstrated that leaves can survive the significant changes in gene expression that are shared these low damaging temperatures if ice nucleation is among and differ between V. vinifera cultivars. prevented through the use of kaolin clay or through eliminating ice-nucleating bacteria16. These studies have Materials and Methods demonstrated that leaves can survive freezing tempera- Plant Material and Treatments tures “by chance” and sporadic damage in vineyards fol- Five different V. vinifera cultivars (“Riesling”, “Cabernet
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